Vol. 456: 113–126, 2012 MARINE ECOLOGY PROGRESS SERIES Published June 7 doi: 10.3354/meps09682 Mar Ecol Prog Ser

Coral community composition and development at the , , in response to strong environmental variations

Gertraud M. Schmidt1,*, Niphon Phongsuwan2, Carin Jantzen1, Cornelia Roder3, Somkiat Khokiattiwong2, Claudio Richter1

1Alfred Wegener Institute for Polar and Marine Research, Am Alten Hafen 26, 27568 Bremerhaven, Germany 2Phuket Marine Biological Center, 51 Sakdidet Road, 83000 Phuket, 34700 King Abdullah University of Science and Technology, Thuwal 23955-6900, Kingdom of Saudi Arabia

ABSTRACT: The Similan Islands, a Thai in the Andaman Sea located near the shelf break, are subjected to frequent (up to several events per hour) and abrupt changes in physico- chemical conditions, particularly during the dry season (NE monsoon, January through April) and to an intense monsoon season with strong surface wave action (May to October). The exposed west slopes of the islands feature more species, but lack a carbonate reef framework. By contrast, the sheltered east sides show a complex reef framework dominated by massive Porites. Our results suggest that the sudden changes in , pH and nutrients (drops of up to 10°C and 0.6 U −1 and increases of up to 9.4 µmol NOx l , respectively) due to pulsed events may rival the importance of surface waves and storms in shaping coral distribution and reef development.

KEY WORDS: Benthic−pelagic coupling · Coral community · Similan Islands · Andaman Sea · Upwelling · Internal waves

Resale or republication not permitted without written consent of the publisher

INTRODUCTION welling is strong, positive fertilizing effects may be counteracted by the negative effects of low tempera- Coral reefs are highly diverse and productive ben- ture, low pH and high nutrient loads favouring algal thic ecosystems thriving in shallow, clear, warm, rather than coral growth (McCook et al. 2001). nutrient-poor, tropical waters (Veron 2000). Many Reef growth is commonly most vigorous on the ex- reefs, however, are subjected to natural disturbances posed offshore (or windward) side of an island (Veron that affect hydrodynamics, light, temperature, nutri- 2000). Along the offshore islands in the Anda man Sea, ents and pH on various scales, e.g. monsoon-driven however, satellite images (www. reefgis. reefbase .org) rainfall, mixing by storms and upwelling of cold, and monitoring studies (Phongsuwan et al. 2008) sug- deep waters (Leichter et al. 1996). Surface gravity gest that reef development is re stricted to the shel- waves can strongly affect coral morphologies and tered east sides, while the west sides appear to be de- reef development in exposed areas (Storlazzi et al. void of reef formations (Fig. 1). 2001). Internal waves have been shown to play an The Andaman Sea features 2 major climatic and important role in the cross-shore exchange of nutri- oceanographic phenomena: a strong SW monsoon ents, larvae and particulate food (Pineda 1991) and from May to October, with strong and heavy can be a source of nutrition for coral reefs (Leichter et rain (Wu & Zhang 1998), and the occurrence of large- al. 2003, Wolanski et al. 2004). However, when up - amplitude internal waves (LAIW) of >60 m amplitude

*Email: [email protected] © Inter-Research 2012 · www.int-res.com 114 Mar Ecol Prog Ser 456: 113–126, 2012

Fig. 1. Typical substrate conditions at about 12 m depth on the (A) west (W 4.1) and (B) east (E 7.1) side of the Similan Islands. See Fig. 2 for site locations

(Osborne & Burch 1980, Jackson 2004) generated by and pH (Levitus & O’Brian 1998), they may select for tidal currents across the shallow ridges of the An- adapted to cope with large fluc tuations in these daman−Nicobar island arc and the reefs NW of Suma- parameters. Further corals may benefit from en- tra (Jackson 2004). The LAIWs travel as waves of de- hanced nutrient supply due to in creasing zooxanthel- pression in packets of 5 to 8 waves eastward across lae densities (Muscatine et al. 1989, Ferrier-Pagès et the deep Andaman basin at speeds of 2 m s−1 al. 2001) and photosynthetic efficiency (Muscatine et (Osborne & Burch 1980) and are observable as rip al. 1989). But higher nutrient also bands on the ocean surface (Jackson 2004). Near the favour the growth of competitively superior macroal- continental shelf break, the rip bands align with the gae (McCook et al. 2001) and enhance bioerosion isobaths and proceed in water shallower than 90 m (Chazottes et al. 2002). Tropical shallow platforms (Jackson 2004), suggesting transformation into waves subjected to intense (wind-driven) up welling have of elevation, breaking and generation of turbulent thus been shown to be devoid of coral reefs (Hallock bores spilling onto the shelf (Vlasenko & Hutter 2002). & Schlager 1986), but moderate and/ or intermittent The resulting diapycnal mixing was shown to enhance upwelling may allow for moderate to extensive reef pelagic production near the shelf break (Jackson development (Andrews & Gentien 1982). 2004, Nielsen et al. 2004) in the swash zone of break- Nevertheless, it cannot be ruled out that physical ing solitons (Vlasenko & Hutter 2002, Jackson 2004). forcing due to storms, mainly during the monsoon The further transport of cold, deep waters due to season, or caused by tsunamis, impacts reef develop- LAIW up to shallow shelf areas, however, has not ment on the exposed western sides of these islands as been proven yet. But 2 recent investigations at the well (Allen & Stone 2005); although the recent Similan Islands, an offshore archipelago in the An- tsunami in 2004 showed only moderate impact on daman Sea located near the shelf break, found Andaman Sea offshore coral reefs (Allen & Stone strong-pulsed upwelling at the exposed western side 2005, Plathong 2005), with <13% of the reefs signifi- of the islands (Roder et al. 2010, 2011), suggesting that cantly damaged, and this damage affecting mostly those LAIW may reach the island chain. These studies the narrow north and south passages between showed differences in the nutritional status of corals islands and not the broad west island faces. growing on the exposed west and sheltered east sides The present study explores the coral abundance during a period of intense, pulsed upwelling. and diversity in coral communities of the Similan This pulsed upwelling might be an important factor Islands subjected to marked differences in tempera- affecting not only the physiology of the corals but also ture fluctuations and monsoonal storm exposure. We the ecology of the coral communities. Low tempera- propose that the pulsed fluctuations due to upwelled tures have been shown to limit reef development waters and the impact of surface waves differentially (Kleypas et al. 1999) and may select for species toler- affect shallow (~7 m) and deep (~20 m), west and east ant to low in areas subjected to up- coral communities and carbonate framework devel- welling of cold water (Brown 1997). Because up - opment. This was tested by comparing coral commu- welled waters can be low in (Levin et al. 1991) nity composition, cover and framework development Schmidt et al.: Coral community response to upwelling and surface wave impact 115

on the west, east, shallow and deep faces of the rocky islands composing the archipelago are aligned islands and relating the biological findings to the from north to south over a distance of about 24 km, physico-chemical characteristics of these habitats. almost perfectly perpendicular to the direction of the LAIW (coming mainly from the west; Jackson 2004), and at an oblique angle (45°) to the SW monsoon MATERIALS AND METHODS (Fig. 2). Their topography and surrounding bathyme- try are characterized by a generally steep slope Study area (>40°) down to 20 m depth along the western sides and a slightly gentler slope (<35°) in the east, with The Similan Islands in the Andaman Sea, Thailand, broad sandy beaches and shallow reefs. The upper are located about 60 km west of the Thai and western slope features large boulders until about 400 km east of the Andaman−Nicobar Islands. The 9 15 m depth before giving away to rubble and coarse sand. The average depth around and between the islands is 70 m (Fig. 2). In the east, the upper slope is shallow (5 to 10 m), with reefs and fine carbonate sands extending about 30 m from the island shores. The deeper slope is steep and covered with corals to a depth of about 30 m. Annual rainfall is 3560 mm and mostly restricted to the SW monsoon between May and October.

Benthic sampling

For the coral community study, 16 localities were selected: 9 were distributed along the eastern sides of the Similan Islands (E 1.1 to E 9.1; Fig. 2) and shel- tered from direct upwelling and monsoon impact; 7 were distributed along the western sides (W 2.1 to W 9.1; Fig. 2) and exposed to the full impact of deep waters and monsoon. Although precaution was taken to obtain a representative dataset, logistical constraints caused some sites to be more clustered (W 8.2. and W 8.3, E 8.1 and E 8.2) than preferable on theoretical grounds. To explore the west–east differ- ences in the benthic composition, one 100 m line transect was established at 14 m depth at each of the 16 localities (marked in each case with W 14 m and E 14 m, respectively) and marked with steel stakes, one at either end. The line-point-intercept method (LPI; Loya 1972) was adopted with measuring points every 50 cm (n = 200 data points transect−1). At each point the benthic component (i.e. scleractinian Fig. 2. Upper left panel: Andaman Sea basin with the Anda - corals, soft corals, macroalgae, rock, sand and rub- man−Nicobar Islands in the west and Thai coast in the east ble) under the transect line was recorded, and the (land area marked grey, isobath scale). Main panel: close-up number of individuals was counted. Scleractinian of the marked box in the upper left panel, with the Similan Islands (marked white) surrounded by shallow (down to corals were identified to species level. To establish 10 m depth, light grey) and deeper reef areas (down to 25 m vertical differences in the composition of the main depth, dark grey), with biological and environmental sam- macrobenthic groups at low taxonomic resolution pling sites: transects only (14 m depth) (d); transects (14 m (no species identification), additional triplicate tran- depth) and temperature (7 and 20 m depth) (M); all parame- sects of 50 m length were conducted at Ko Miang on ters including transects at 7, 14 and 20 m depth (J) at the central island Ko Miang (W 4.1 and E 4.1) (figure modified both west (W 4.1) and east (E 4.1) sides at 20 m and after Jackson 2004) 7 m depth (W 20 m and E 20 m, W 7 m and E 7 m, 116 Mar Ecol Prog Ser 456: 113–126, 2012

respectively). These transect lines were positioned measured in 1 min intervals with a CTD (Seacat SBE one after another along the respective isobath with a 19plus, Sea-Bird Electronics) deployed at 20 m depth distance of 10 m between the end of one and the on the west side (W 4.1) of Ko Miang (Fig. 2) in March beginning of the next. Again, the LPI method was 2007 for 4 wk. Light loggers (Onset pendant light log- adopted as described above (n = 100 data points ger: 0 to 320 000 lux [lm m−2]) were deployed on both transect−1, analysis of similarity [ANOSIM] between sides of Ko Miang (W 4.1, E 4.1) at 2 depths (20 and tripicate transects to exclude auto-correlation; see 7 m) about 20 cm above the substrate recording light Table S5 in the supplement at www.int-res.com/ values every minute from December 2007 until April articles/ suppl/m456p113.pdf) . 2008. The loggers were cleaned daily to keep fouling Carbonate framework development was assessed organisms from interfering with light measurements. on both west and east sides of islands 4.1 and 8.1 (at Additionally, a photosynthetic active radiation (PAR, 4.1 at 7 and 20 m depths and at 8.1 at 14 m depth) µmol quanta m−2 s−1) sensor (Biospherical Instru- from scaled photographs, showing the elevation of ments) was mounted on a CTD (SEACAT, SBE the coral framework above its basement (sediment or 19plus, Sea-Bird Electronics) in January 2008 over a rock) and a measuring stick positioned perpendicular period of 20 d on the west side of Ko Miang (W 4.1) at to the isobaths in front of the framework. Images 20 m depth. were taken every 5 m along the transects (where applicable, i.e. corals were present). The height of the framework was calculated by image analysis Chemical measurements with the software ImageJ as the closest distance (in cm) between the top 10 tips of corals and the base- A total of 89 water samples was collected by ment. A total of 207 framework measurements was SCUBA during daily dives at Ko Miang in February carried out — 21, 67 and 59 in the west at 7, 14, and and March of 2007 and 2008 (Fig. 2; at W 4.1: 21 sam- 20 m depth, respectively, and 16, 28 and 16 each in ples at 20 m, 18 samples at 7 m depth; at E 4.1: 25 the east at 7, 14 and 20 m depth, respectively. samples each at 20 and 7 m depths). Samples were taken with 1 l PE-bottles about 1 m above the reef substrate in the vicinity of the temperature loggers. Physico-chemical sampling The sampling time was recorded on each occasion for later correlation with water temperature. Immedi- Temperature measurements ately after collection, water samples were filtered through pre-combusted and pre-weighed glass-fibre A total of 20 temperature recorders (TidbiT v2, filters (Whatman GF/F, 45 µm) for determination of Onset computers; resolution 0.2°C within a range of 0 total suspended matter (TSM). The filters were kept to 50°C) recording temperature at 6 min intervals frozen before drying at 50°C and determining dry were deployed at 2 depths (20 and 7 m) and expo- of TSM gravimetrically (Mettler, AT21 Com- sures (west and east) at 5 study sites (2.1, 4.1, 7.1, 8.1 parator, 1 µg accuracy). Aliquots of the filtrate were and 8.3; Fig. 2). Loggers were attached about 20 cm stored in sterile polypropylene bottles after poisoning above the substrate and kept for 21 mo from Febru- them with mercuric chloride (Kattner 1999) until ary 2007 to November 2008. Additional temperature inorganic nutrients (nitrate, nitrite, ammonium, phos- loggers were deployed at the island Ko Miang (W 4.1 phate and silicate) were analyzed according to and E 4.1) at 7, 14 and 20 m depths logging for 4 mo Grasshoff et al. (1999) and Parsons et al. (1989) in a from December 2007 through March 2008. Intercali- spectrophotometer (GBC Model UV/VIS981 with bration of the TidbiT loggers after the long-term autosampler Model FS3000 in 2007, and Evolution III deployment showed small temperature differences autoanalyzer, Alliance Instruments, in 2008). Further between loggers (max. 0.8°C) contrasted by up to filtrate aliquots were transferred to pre-combusted 10°C temperature variations in the course of the glass ampoules spiked with phosphoric acid and pulsed upwelling events. flame sealed for determination of dissolved organic carbon (DOC). DOC samples were analyzed by means of high temperature catalytic oxidation using CTD and light measurements a Dohrman DC-190 Total Organic Carbon Analyzer equipped with a platinum catalyst. Before injection Temperature, salinity, , oxygen, pH, chlo - into the furnace, the acidified samples were decar- rophyll a fluorescence and optical backscatter were bonated by purging with oxygen. The evolving CO2 Schmidt et al.: Coral community response to upwelling and surface wave impact 117

was purified, dried and detected by a non-dispersive residuals into positive (warm) and negative (cold) infrared detection system. values, and summing up the values for the cold resid- uals. Given the highly skewed distribution of the temperature data and the sensitivity of the arithmetic Data processing and statistical analysis mean to outliers, it was appropriate to use the most common (or mode) temperature to represent the Biological and environmental data were tested for average. The moving average was calculated using the assumption of normality and homogeneity of a slide function (by Jos van der Geest; www. variances using Kolmogorov-Smirnov and Levene’s math works. com/matlab central/fileexchange/ 12550) tests, respectively, and subjected to parametric and with a 1 d time window for the mode value. The daily non-parametric analyses, as required. sum of cold residuals was divided by the number of Transect data were processed as percentage samples per day. As not all loggers were recording abundances per site and analyzed with the software without failure at all sites, the calculation of DDC was PRIMER v6 for non-parametric multivariate datasets done for the period when data were available from (Clarke & Gorley 2006). Analysis of similarities all sites and depths (20 wk, February 2007 to July (ANOSIM) permutation tests based on Bray-Curtis 2007, covering the SE and SW monsoon periods in similarities were used to detect spatial differences roughly equal proportion). The relationship between in substrate cover and species compositions be- physical (DDC), chemical (nutrients) and biological tween island sides (1-way analysis with 25 iteration (coral community composition and cover) descriptors steps). It was further used to clarify depth-depen- was assessed using linear-regression analyses. dent benthic cover and distribution of substrate Possible temperature differences (monthly minima, types on the west and east sides of Ko Miang (2- maxima and mode values) between sites correspond- way-crossed design implicating the differing expo- ing to the same upwelling exposure (e.g. W 20 m) sure depending on orientation: W versus E; depth: were tested with Student’s t-tests (Table S1 in the 20 versus 7 m). ANOSIM calculates a global R sta- supplement at www.int-res.com/ articles/ suppl/m456 tistic that reflects the differences in variability be - p113.pdf), and data for all sites that were not statisti- tween groups as compared to within groups (so R cally different (at p = 0.01) were pooled for further values are proportional to differences between the analyses. Temperature data, nutrient concentrations groups) and checks for the significance of R using and light recordings were statistically tested for permutation tests (Clarke & Gorley 2006). Non-met- differences between west and east using non- ric multidimensional scaling (NMDS) was used to parametric Kruskal-Wallis ANOVA by ranks. Linear- further describe the benthic communities. Based on regression analyses were undertaken to test the rela - a similarity matrix, NMDS generates plots in which tionships between both chemical and physical the distance between points is proportional to their parameters in the water as the dependent variables, degree of similarity (Clarke & Gorley 2006). Similar- ity percentage (SIMPER) analyses were consulted to assess the respective contributions of substrate types and coral species to the similarities and dis- similarities within and among the west and east sites studied. Descriptive coral community factors such as the Shannon index, evenness and species richness (Rogers 1993) were calculated for every site and tested for exposure (west vs. east) using Student’s t-tests. The effect of side (west and east) and depth (7, 14 and 20 m) on coral framework development was analyzed using ANOVA, with side and depth as treatment factors; post hoc, pair- wise comparisons were performed via Tukey’s HSD tests. The calculation of degree days cooling (DDC; °C d) Fig. 3. NMDS ordination of coral communities at the Similan Islands based on species abundance data (%) and Bray- as a site-specific indicator of the up welling involved Curtis similarities from 1 × 100 m transect at 14 m depth at the following steps: decomposing the temperature each study site. West (Z) and east (M) sites (see Fig. 2) data into moving average and residuals, splitting the grouped in separate clusters 118 Mar Ecol Prog Ser 456: 113–126, 2012

with temperature as the independent variable, fol- RESULTS lowed by a Student’s t-test to examine their statistical significance. If not stated otherwise data are always Reef data displayed as means (±SE). Coral community composition

Table 1. Coral diversity indices (Shannon index [Hk], even- A total of 144 species was re- ness [Ek], species richness [S]), and coral cover (as a fraction of hard substrate) determined from 1 × 100 m transect at corded, belonging to 40 genera and 17 families 14 m depth at each study site (all sites). At island Ko Miang (Tables S2 & S3 in the supplement). Coral species (Sites W 4.1 and E 4.1, see Fig. 2) additional determination of composition differed between island sides (ANO - coral cover at 20 m and 7 m depth from in each case 3 × 50 m SIM, 1-way analysis: west versus east: global R = transects (mean ± SE). Linear regression model with H , E , k k 0.585, p < 0.001, dissimilarity 83.2%; Table S4) as S and coral cover as dependent and degree days cooling (°C d) as independent variables (n = number of samples; seen also in the distinct clustering in the NMDS plot significance levels are *0.05 > p ≥ 0.01, **0.01 > p ≥ 0.001) between west and east sites (Fig. 3). In the west, a higher species diversity (t-test, p < 0.01), richness Depth Index Site location n R2 p (t-test, p < 0.02) and evenness (t-test, p < 0.04; Table (m) West East 1) was found compared to in the east. In the east all sites where characterized by a dominance of Porites All sites species (64.2% cover as a fraction of total coral 14 Hk 2.69 (0.15) 2.03 (0.13) 10 0.4 * cover compared to 15.7% in the west; Table S2 Ek 0.74 (0.04) 0.63 (0.04) 10 0.07 0.46 S 38.4 (2.4) 27.3 (3.4) 10 0.63 ** & S3). The within-west and within-east similarities Coral cover 0.36 (0.04) 0.49 (0.05) 10 0.13 0.29 in species composition were low (24.3 and 31.9%, Ko Miang respectively; Table S4), due to a variable number of 20 Coral cover 0.32 (0.09) 0.79 (0.08) 6 0.42 0.08 rarer species mainly within the genera 14 0.35 0.58 7 0.54 (0.04) 0.54 (0.03) (28.6% cover as a fraction of total coral cover in the west and 11.5% in the east) and Porites distributed

A 100

80 Living corals Soft corals 60 Sponge Algae 40 Cover (%) Dead coral 20 Rock Sand & rubble 0

100 B

80

60 Solitary Laminar 40 Branching

Proportion of Proportion Encrusting 20 Massive coral morphologies (%) 0 7 m 14 m 20 m 7 m 14 m 20 m West East Fig. 4. Benthic composition at Ko Miang on exposed west (W 4.1) and sheltered east (E 4.1) sites (see Fig. 2), grouped by depth: 7, 14 and 20 m: (A) general benthic composition and (B) coral morphologies as fractions of total number of living colonies Schmidt et al.: Coral community response to upwelling and surface wave impact 119

unevenly between the sites, particularly in the west structures were only found in the west, while in the (Tables S2 & S3). east hard substrate consisted exclusively of dead coral (Fig. 4A, Table S6).

Benthic substrate composition Coral framework and morphologies From the 2 sides (west, east) and 3 depths investi- gated at Ko Miang (7, 14 and 20 m), the lowest living A dense 3-dimensional coral framework character- coral cover was found at W 20 m (ANOSIM, 2-way- ized the east, whereas in the west hard corals were dis- crossed analysis: W 4.1 versus E 4.1: global R = 0.639, tributed as solitary colonies without developing an p < 0.02; Fig. 4A). Significantly higher living coral actual carbonate framework (ANOVA, Tukey HSD- cover was found at W 7 m (35.7 ± 5.6% versus 12 ± tests: W versus E, p < 0.001; Fig. 5, Table S7). This was 4.4% at 20 m depth), E 20 m and E14 m (36.7 ± 4.6% especially distinct at W 20 m and W 7 m, whereas at W at 20 m depth and 33.6% at 14 m depth versus 18.7 ± 14 m depth the framework was higher (ANOVA, 5.5% at 7 m depth; 20 m versus 7 m: global R = 0.37, Tukey HSD-test: p < 0.001; Fig. 5, Table S7). Coral p < 0.05; Fig. 4A). Living coral cover was the second morphologies differed significantly be tween sides most powerful contributor to the dissimilarity of (ANOSIM 2-way-crossed analysis: W versus E, global 72.5% between west and east, with a contribution of R = 0.311, p < 0.05) and depths (7 versus 20 m, side data 25.1%; the most important contribution to this dis- pooled, global R = 0.253, p < 0.05) (Fig. 4B). The domi- similarity between west and east was achieved by nance of massive and encrusting colonies in the west sand and rubble with 35.9%, followed by rock and of branching species in the east of Ko Miang fell (17.9%) in third position. At 14 m depth, differences short of being significant (t-test, p = 0.064 and p = 0.1, in the benthic composition failed to be significant respectively). Large massive and encrusting hard coral between west and east sides (ANOSIM, 1-way analy- species sparely covered areas at W 20 m, and small sis: global R = 0.079, p = 0.22; Table S5 in the supple- colonies of all morphological types grew very close to ment at www.int-res.com/ articles/ suppl/ m456 p113 each other on the rocks in shallower west waters (Fig. .pdf) due to si milar distributions of total hard sub- 4B). Here, branching hard corals, especially within the strate consisting of dead coral, living coral and rock genera Millepora and Acropora, often displayed flat- (with 67.7 ± 6.6% in the west and 72.8 ± 3.3% in the tened morphologies with pancake-like broadened east), and sand including rubble (with 29.8 ± 6.9% in bases and strongly reduced ramification (Fig. 1A). the west and 25.9 ± 3.3% in the east). Living coral cover exhibited higher differences between the west (25.6 ± 4.2%) and east (35.9 ± 4.6%) sides. Rock Physico-chemical environment

The pattern of high- and low-variability periods and order of magnitude in amplitude in the tempera- ture time series was consistent among all sites of the same depth and orientation (Fig. 6, cf. synchronous monthly mode, minimum and maximum temperature values, Student’s t-tests: Table S1). This is also reflected by the differences between mean values and ranges (maximum to minimum temperature) of monthly temperature between west and east sites (Table 2; Kruskal-Wallis W 20 m versus E both depths: p < 0.00; Table S8). Mode values differed only between W 20 m and E 7 m sites (Table 2; Kruskal-Wallis, p < 0.01; Table S8) and showed small (<3.5°C) seasonal differences, irrespective of side or depth. The low seasonal variability contrasts with the Fig. 5. Coral framework at the west and east sides of island high variability found at higher frequencies, as Sites 4.1 (7 and 20 m) and 8.1 (14 m) (see Fig. 2) grouped by reflected by the large differences between mode and depth: 7, 14 and 20 m. Central tendency box plots show me- dian with 25th and 75th percentiles and non-outlier range; minima values showing declining temperature fluc- extremes: dots tuations: W 20 m > W 7 m > E 20 m > E 7 m (Fig. 6, 120 Mar Ecol Prog Ser 456: 113–126, 2012 ) values at 5 d Nov Mar Jul Nov Jul ) and mode ( d ), maximum ( s nd 7 m depth (orientation south to north). Blank Nov Mar Jul Nov Mar Jul Nov Mar Jul Nov Mar Jul W 4.1 W 4.1 W 8.1 W 8.3 Nov Mar Jul Nov Mar Jul W 2.1 W 4.1 W 4.1 W 8.1 W 8.3 W 2.1 W 4.1W 2.1 W 4.1 W 4.1W 2.1 W 8.1 W 4.1 W 8.3 W 8.1 W 8.3 periods are missing values due to lost or broken line in each panel indicates change of year 2007 to 2008 loggers. Vertical Nov Mar Jul Nov Mar Jul West 20 m West 7 m West East 20 m East 7 m Mar 32 30 28 26 24 22 20 34 32 30 28 26 24 22 20 32 30 28 26 24 22 20 32 30 28 26 24 22 20 Temperature (°C) Fig. 6. Temperature recordFig. 6. Temperature covering 21 mo along the Similan Islands (March 2007 to November 2008): monthly minimum ( west (W 2.1, W 4.1, W 7.1, W 8.1, W 8.3) and east (E 2.1, E 4.1, E 7.1, E 8.1, E 8.3) sites (see Fig. 2), respectively, in 20 a west (W 2.1, W 4.1, 7.1, 8.1, 8.3) and east (E E sites (see Fig. 2), respectively, Schmidt et al.: Coral community response to upwelling and surface wave impact 121

Table 2). Corresponding DDCs showed 5-fold higher tistics did not support temperature-dependent varia- values at W 20 m compared to E 7 m (Kruskal-Wallis tions in optical backscatter and chl a fluorescence test: p < 0.001; Table S8) and about 2- and 3-fold (Fig. S1 in the supplement). higher values than at W 7 m and E 20 m, respectively Highest light intensities (lux, l m m−2), were found (Table 2). at E 7 m and lowest at W 20 m. Light conditions were Fig. 7 shows a time series section of raw data at significantly different in the west and east at both W 20 m at Ko Miang during strong temperature depths (7 and 20 m) (Kruskal-Wallis test, p < 0.001; fluctuations. Synchronization of abrupt temperature Table S9A), with over 3-fold higher light values in de creases of up to 5−9°C occurred with drops in the east during midday and a longer lasting light oxygen of down to 12% (down to environment at W 7 m at the end of the day (Fig. 8). 21.8 µmol l−1), in pH of up to 0.6 U (down to 7.75) and This pattern can be explained by the topographical increases in salinity of up to 1.5 to values of 34.4. Sta- characteristics of all the islands, with high, steep slope-shaped west sides shading the Table 2. Summary of temperature data (°C): monthly mean, mode, range west for longer than the east and flat- (maximum to minimum temperature), and degree days cooling (DDC, °C d, tened island topography in the east. calculated for a 20 wk period) (±SD) for all sites recorded along the Similan Is- During a period of high temperature lands (5 sites per side: W and E; depths: 20 and 7 m) over 21 mo (February 2007 variations in January 2007, PAR to November 2008) and for Ko Miang (west side: W 4.1, east side: E 4.1, depths 20, 14 and 7 m; see Fig. 2) over 5 mo (December 2007 through March 2008) never exceeded 141.5 µmol quanta m−2 s−1 at W 20 m, with a mean of −2 −1 West East 102.5 ± 3.4 µmol quanta m s . 20 m 14 m 7 m 20 m 14 m 7 m Nutrient concentrations revealed significant differences between the All sites west and east for nitrate and nitrite, as Mean 28.5 (0.7) 28.8 (0.6) 28.8 (0.5) 29.1 (0.5) well as for silicate (Kruskal-Wallis test, Mode 28.7 (0.6) 28.9 (0.1) 28.8 (0.6) 29.0 (0.6) Range 5.2 (1.7) 4.3 (1.7) 2.7 (1.3) 2.1 (0.1) p < 0.001 and p < 0.04, respectively). DDC −58.3 (1.9) −31.6 (3.8) −24.6 (2.5) −11.8 (4.9) Mean concentrations of silicate were Ko Miang >60% higher at W 20 m than at Mean 28.0 (0.8) 28.3 (0.7) 28.6 (0.5) 28.4 (0.5) 28.4 (0.4) 28.6 (0.5) E 20 m, supported by an increase of Mode 28.2 (0.4) 28.1 (0.5) 28.4 (0.4) 28.1 (0.4) 28.2 (0.6) 28.1 (0.5) nitrate and nitrite (40%) and of phos- Range 5.6 (1.1) 4.8 (1.1) 4.3 (1.1) 3.4 (0.7) 2.6 (0.8) 2.8 (1.0) DDC −70.6 −39.0 −16.3 −23.0 −9.3 −9.3 phate (50% higher at W 20 m than at E 7 m) concentrations (Table 3). In

Fig. 7. (A) Raw data time series of a CTD recording from a 48 h section in March 2007 (temperature, pH, oxygen concentration, salinity) at Ko Miang west at 20 m depth (logging interval: 1 min). (B) Linear-regression analysis, with pH, oxygen concentra- tion and salinity as dependent variables, and temperature as the independent variable 122 Mar Ecol Prog Ser 456: 113–126, 2012

Link between coral community parameters and DDC

Diversity (Shannon index) and species richness de - ter mined at the intermediate depth of 14 m in the west and east exhibited a positive relationship with DDC (Table 1). Living coral cover as a fraction of the available hard substrate determined at 7, 14 and 20 m depths in the west and east may be inversely related to DDC, but this correlation failed to be sig- nificant (Table 1).

DISCUSSION Fig. 8. Composite daily light curves at Ko Miang west (W 4.1) and east (E 4.1, see Fig. 2) at 20 and 7 m depths for a period of The Similan Islands reveal a lack of 30 d (February to March 2007; logging interval: 1 min) framework development along their western sides, in contrast to the complex 3-dimensional Table 3. Environmental parameters determined from water samples at Ko Mi- coral framework in the east. The de- ang (W 4.1 and E 4.1) displayed as means (±SE) and linear regression model velopment of coral reefs in general with environmental parameters as dependent and water temperature (at time has been reported to be undermined of sampling) as independent variables (n = number of samples; significance level is ***p < 0.001) by cold water influence (Burns 1985, Kleypas et al. 1999). Although several tropical corals are known to occur Units Depth Depths pooled 20 m 7 m n R2 p over a wide geographical range of temperatures (e.g. up to 12°C differ- West, W 4.1 ences in maximum summer tempera- −1 Silicate µmol l 6.86 (1.29) 3.84 (0.67) 36 0.72 *** tures for species co-occurring in the Phosphate µmol l−1 0.42 (0.08) 0.21 (0.03) 35 0.41 *** Nitrate + nitrite µmol l−1 2.11 (0.47) 0.74 (0.15) 36 0.65 *** Arabian Sea and Lord Howe Island, Ammonium µmol l−1 1.14 (0.22) 0.92 (0.13) 30 0.01 0.66 Australia; Hughes et al. 2003), and Dissolved ppm 1.11 (0.12) 1.02 (0.07) 34 0.03 0.36 can tolerate large annual ranges of organic carbon temperature (up to 25°C) and survive Suspended mg l−1 12.40 (0.68) 13.75 (1.03) 37 0.09 0.07 particulate matter severe cold periods (13°C for several days; Coles & Fadlallah 1991), cold East, E 4.1 Silicate µmol l−1 4.33 (0.39) 3.06 (0.30) 48 0.50 *** water stress (6 to 10°C under normal Phosphate µmol l−1 0.30 (0.05) 0.23 (0.03) 42 0.03 0.18 conditions) may disrupt the sensitive Nitrate + nitrite µmol l−1 0.90 (0.16) 0.56 (0.17) 47 0.38 *** association between corals and their −1 Ammonium µmol l 0.98 (0.12) 0.92 (0.09) 35 0.21 0.06 en do symbiotic zooxanthellae and re- Dissolved ppm 1.58 (0.31) 1.03 (0.07) 43 0.01 0.56 organic carbon sult in a de creased fitness and growth Suspended mg l−1 13.80 (0.78) 12.88 (0.72) 44 0.12 0.06 performance of the coral host (Coles & particulate matter Fadlallah 1991, Gates et al. 1992, Saxby et al. 2003). The reduced coral cover in the west at 20 m depth and shallow waters the differences may be still noticeable the absence of reef framework in the west may there- but are far less pronounced and statistically not signif- fore be partly due to the observed temperature fluc- icant. Nutrient concentrations exhibited a negative tuations. The cold temperatures in the present study, re lationship with temperature when cor related to the however, were only one stressor out of several co- in situ temperature during sampling (Table 3). No sig- occurring environmental factors. Temperature was nificant differences were found between the different negatively correlated with nutrient input (Table 3) sides of the island in ammonium concentration, dis- and salinity, and positively with pH and oxygen con- solved organic carbon or suspended particulate centration (Fig. 7). Thus, the cold water masses matter which varied independently of temperature reaching the west of the Similan Islands may be de- variations (Table 3, Table S9B in the supplement). rived from sub-pycnocline sources containing re- Schmidt et al.: Coral community response to upwelling and surface wave impact 123

mineralized nutrients (Jackson & Williams 1985) due & Davies 1979, Ferrier-Pagès et al. 2000). Values of to and decomposition processes in areas pH decreased during cold-water intrusions in the isolated from additional oxygen supply (Levin et al. west (up to 0.6 U; Fig. 7). This effect in com bination 1991). The covariance of temperature with these en- with reduced light intensities (Fig. 8) may be the main vironmental parameters (Fig. 7, Table 3) allowed an reason for the significantly reduced coral growth at W assessment of the physico-chemical environment 20 m depth (Schmidt et al. unpubl. data), as both pro- from temperature alone for periods where no other cesses are tightly coupled in zooxanthellate corals data were available. Exceptions were the dissolved and their efficiency suffers from lowered pH and light organic matter and suspended particulate matter levels (Marubini et al. 2001). This might also be a ma- concentrations (see also optical backscatter; Fig. S1), jor reason for the inability of the corals in the west to which were independent of temperature and similar develop a reef framework (Manzello et al. 2008). between west and east. Reduced oxygen and high The pulsed extreme conditions in the chemical and nutrient concentrations in the sub- waters physical environment are replaced each time within transported into shallow areas may possibly have led 15 to 30 min, again by warm surface water (see Fig. 7; to a mutual compensation of depletion (low oxygen) nearly identical mode temperature values in the west and production processes (plankton production due and east; Table 2). The intensity of these fluctuations to higher nutrient concentrations; Eppley et al. 1979) increases with depth (7 m < 14 m < 20 m), but does not in the west. This could have been a reason for the seem to cause severe physiological damage or mortal- lack of difference in dissolved organic matter concen- ity as observed for long-term disturbances following trations between west and east. The similar particu- cold spells (Coles & Fadlallah 1991) or eutrophication late matter concentrations appeared inconsistent (Szmant 2002). Monsoonal storms, on the other hand, with the differences in the physical oceanographic occur at monthly or seasonal frequencies (Wu & Zhang variables and the varying light conditions between 1998) and last for days. Their impact diminishes with west and east sides. This could be explained by depth. When looking at the intermediate depth of higher suspended particulate loads in the west than 14 m in the west, the coral framework was higher than in the east caused by higher currents (Roder et al. in deep (20 m) and shallow (7 m) waters, and high 2011) and due to more intense resuspension. Mean coral diversity was found in contrast to the sheltered nutrient concentrations for nitrate, nitrite and phos- eastern reefs (Table 1). In the east species diversity phate in the west were above the average concentra- may be lower in the absence of disturbance due to tions of most tropical reefs (Table 3, Kleypas et al. competitive exclusion in an equilibrated system (Con- 1999). During periods of high temperature fluctua- nell 1978), with high coral cover but less species dom- tions (February, March) they were close to or even inating the communities and no available free sub- above the extreme values assessed for coral reef com- strate for new settlers (no bare rock in the east; munities (Kleypas et al. 1999). Increased nutrient Table S6). In the west, however, the seasonal alterna- concentrations entail neutral or positive effects on tion of temperature fluctuations (January through coral nutrition, physiology and zooxanthellae concen- April) and monsoonal surface waves (May through trations (Muscatine et al. 1989, Ferrier-Pagès et al. October) may be a disturbance which represents a 2001). The combination of higher velocities selective regime (Karlson 1980) to which organisms and nutrient concentrations can enhance coral nutri- adapt and generate a variety of competitive mecha- ent uptake (Hearn et al. 2001) and photosynthesis nisms (Karlson & Hurd 1993). This non-equilibrium (Szmant 2002). Accordingly, higher pigment concen- state may reset succession, with regularly new settling trations in western corals were indicative of their sim- corals on the available free substrate (bare rock in the ilar net photosynthetic rates compared to sheltered west; Table S6), and thus enhance coral development eastern corals (Jantzen 2010). Several coral species of and coral species diversity (Connell 1997). different morphology and growth rates along the Going deeper to 20 m depth along the western Sim- Similan Islands displayed higher pigment concentra- ilan Islands, the reef assemblage is impoverished, tions, protein content and biomass under the influ- with single corals growing apart from each other ence of increased nutrient concentrations and higher (Figs. 4B & 5). This is reminiscent of coral commu - planktonic food supply in the west (Roder et al. 2010, nities described for upwelling-influenced sites domi- 2011). However, these positive effects on coral nutri- nated by only one or a few species, such as mainly tion and photosynthetic performance may be small Porites, Acropora. and Pocillopora. (Benzoni et al. compared to the negative direct effects of nutrients 2003). Slow-growing, massive and sub-massive spe- and low pH on coral calcification and growth (Kinsey cies dominated the community here (Fig. 4, Tables S2 124 Mar Ecol Prog Ser 456: 113–126, 2012

& 3). Corals of this type are often described as stress- species-rich communities where regular disturbance tolerators (Riegl & Piller 2000, Veron 2000, Benzoni et produces a highly successional community structure. al. 2003), with high adaptive tolerance to different types of environmental stress (Marshall & Baird 2000, Alutoin et al. 2001, Fabrizius et al. 2011). This was Caveats to the conclusions also shown by Roder et al. (2011) who found high metabolic plasticity in the species Porites lutea and The western Similan Islands were found to be ex- Diploastrea heliopora to the fluctuating chemical posed to temperature fluctuations (see also Roder et conditions in the west of the Similan Islands. The al. 2010, 2011) which are more frequent and severe general abundance of branching species was reduced than reported earlier elsewhere (Leichter et al. 1996, in the west compared to in the east (Fig. 4B); how - 2003), and rank among the largest ones so far re- ever, Acropora species showed comparatively higher ported in tropical shallow reef areas above 30 m depth abundances in the west. Possibly Acropora corals (Wolanski et al. 2004, Sheppard 2009). Seasonal vari- were able to benefit more than other coral species ations, revealing the strongest temperature fluctua- from the changes in environmental conditions be- tions during the late NE monsoon (March; Fig. 6) may tween upwelling and monsoon-impact periods. Most be related to variations in the depth and strength of of them are fast-growing species (Veron 2000) and the pycnocline: the shallow pycnocline during the NE able to recover rapidly from disturbances and spread monsoon corresponds to the strongest LAIW activity by using broken coral fragments as new settling (Nielsen et al. 2004). The pulsed, short-term fluctua- colonies (Highsmith 1982). Light-catching table-like tions of temperature to the order of minutes, periodic morphotypes of branching colonies which would occurrences in several events per day (Fig. 7) and sea- have been due to the reduced light conditions with sonal variations (Fig. 6; see also Wolanski et al. 2004 increasing depth (Macintyre & Smith 1974) were rare and Storlazzi et al. 2003) indicate that they may be in the west. This indicates that hydrodynamics in the caused by LAIW reaching these shallow-water areas. west, due to the high current speeds correlated with The especially high temperature variability in 2007 cold water (Roder et al. 2010) and due to surface grav- compared to 2008 (Fig. 6) may be related to the untyp- ity waves, may have reduced the number of sheltered ical positive Indian Ocean Dipole event in 2007 (Be- sites for these exposed growth forms. Especially the hera et al. 2008) with stronger upwelling events shallow (7 m), western corals showed growth patterns (Webster et al. 1999) and likely internal waves. as described for high-wave-energy areas (Storlazzi et Even though LAIW seem to be the likely source of al. 2001, 2003) nestled and disjointed directly to the the observed temperature fluctuations, other possible granite basement with robust or fast-growing colo- factors, such as current-driven advection of cold wa- nizing species. However, the impact of surface ters (Andrews & Gentien 1982) or seasonal wind- gravity waves can only be estimated as we lack driven upwelling (D’Croz & O’Dea 2007), cannot be knowledge of their actual intensity and maximum excluded. Research in this area has just started and depth range for our study area. We suppose that, in needs to be expanded further to include data not only contrast to most other reef sites, coral morphologies, on the NE monsoon period but also the SW monsoon, species distribution and reef development in the west to complement our knowledge on surface wave im- are affected by both hydrodynamics in shallow areas pacts and to disentangle the differential influences of causing coral breakage and leading to hampered upwelling and surface waves on coral reef develop- 3-dimensional reef development (Fig. 5, Grigg 1998) ment. In addition, verification of the primary drivers of and the highly fluctuating physico-chemical condi- the temperature fluctuations — these may be currents, tions with increasing depth. or internal waves — would complement the pre- In summary, the composition of a coral community sent approach and set it in its oceanographic context. reflects the interaction of the governing physical, chemical and biological drivers (De Vantier et al. Acknowledgements. The research for the present study was funded by the German Research Foundation (DFG, RI 1998). The coral communities growing along the 1074/7-1), the National Research Council of Thailand western Similan Islands are exposed to a stressful (NRCT), and the German Federal Ministry for Education physico-chemical environment. They appear to be and Research (BMBF, Grant Number: 03F0608B, Bioacid adapted to mechanical disturbances, such as strong 3.2.3, Coral calcification in marginal reefs). The authors thank the Phuket Marine Biological Center (PMBC) and the surface waves, and they deal successfully with the Similan Islands National Park staff for field assistance, as pulsed frequent supply of sub-pycnocline waters into well as Tobias Funke for technical, and Matthias Birkicht their low-light environment. They appear to exist in and Dorothee Dasbach for laboratory assistance. Schmidt et al.: Coral community response to upwelling and surface wave impact 125

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Editorial responsibility: Charles Birkeland, Submitted: July 27, 2010; Accepted: February 20, 2012 Honolulu, Hawaii, USA Proofs received from author(s): May 25, 2012